Indirect Defense in Sorghum: Attraction of Natural Enemies to Aphid-Infested Plants Varies among Cultivars

doi:10.21203/rs.3.rs-3408500/v1

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Indirect Defense in Sorghum: Attraction of Natural Enemies to Aphid-Infested Plants Varies among Cultivars

https://doi.org/10.21203/rs.3.rs-3408500/v1

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Herbivore-induced plant volatiles (HIPVs) are an indirect defense used by plants to attract natural enemies and reduce herbivory by insect pests. In many crops including sorghum (Sorghum bicolor), little is known about genotypic variation in HIPV production or how this may affect natural enemy attraction. In this study, we identified and quantified HIPVs produced by 10 sorghum cultivars infested with a prominent aphid pest, the sorghum aphid (Melanaphis sorghi Theobald). Volatiles were collected using dynamic headspace sampling techniques and identified and quantified using GC-MS. The total amounts of volatiles induced by the aphids did not differ among the 10 cultivars, but overall blends of volatiles differed in composition. Most notably, aphid herbivory induced higher levels of methyl salicylate (MeSA) in two cultivars. In addition, four cultivars did not change in the volatile emissions after herbivory. Dual-choice olfactometer assays were used to determine preference of the aphid parasitoid, Aphelinus nigritus, and predator, Chrysoperla rufilabris, between plants of the same cultivar that were un-infested or infested with aphids. Two aphid-infested cultivars were preferred by natural enemies, while four other cultivars were more attractive to natural enemies when they were free of aphids. The remaining four cultivars elicited no response from parasitoids. Our work suggests that genetic variation in HIPV emissions greatly affects parasitoid and predator attraction to aphid-infested sorghum and that screening crop cultivars for indirect defenses has the potential to improve the efficacy of biological control.

Sorghum bicolor L.

Melanaphis sorghi Theobald

sorghum aphid

herbivore-induced plant volatiles

tri-trophic interactions

intraspecific variation

One of the most striking ways that plants can defend themselves from herbivory is through indirect defenses that attract predatory and parasitic arthropod ‘bodyguards’ to kill insect herbivores (Heil 2008, Aljbory and Chen 2018, Pearse et al. 2020). Herbivore-induced plant volatiles (HIPVs) are odor cues emitted by plants in response to herbivore damage that can assist natural enemies in locating their prey. The emission of HIPVs can lead to higher natural enemy abundances, lower herbivore abundances, and increased plant fitness (Turlings et al. 1990, Rasmann et al. 2011, Kessler and Baldwin 2001, Schuman et al. 2012). HIPVs are emitted as blends of volatile compounds produced by several biosynthetic pathways (Dudareva et al. 2013) and attraction of natural enemies to these HIPVs has been demonstrated in a variety of crop plants (Stenberg et al. 2015). There is great potential for HIPVs to improve biological control and sustainable agriculture (Mitchell et al. 2016, Kansman et al. 2023) – however, to implement indirect defenses into pest management, it is crucial to understand the variation in induction and expression of these defenses in crop plants.

Plant breeding has selected for crop varieties that vary in the expression of many different agronomic and resistance traits. Notably, several studies have highlighted intraspecific genetic variation in HIPV emission in crop species including cotton (Loughrin et al. 1995), maize (Gouinguene et al. 2001, Degen et al. 2004), rice (Lou et al. 2006), cucumber (Kappers et al. 2010), cranberry (DeLange et al. 2019), cabbage (Poelman et al. 2009), and lima bean (Ballhorn et al. 2008). Screens for quantitative and qualitative variation in HIPV blends have highlighted important differences among crop varieties – for example, the volatile terpenoid compound (E)-β-caryophyllene is produced by specific European maize lines, but not by North American maize lines (Degen et al. 2004). Such variation in HIPV emission can lead to differences in the attraction of natural enemies and, in turn, the efficacy of biological control (Kappers et al. 2011). European maize lines attacked by Western corn rootworm (Diabrotica v. virgifera) producing (E)-β-caryophyllene were more attractive to entomopathogenic nematodes than North American varieties (Rasmann et al. 2005), leading to increased attraction of entomopathogenic nematodes, higher nematode infection rates, and lower abundances of rootworm adults and larvae. Restoring the ability to produce (E)-β-caryophyllene via genetic transformation allowed for decreased root damage and herbivore abundances in the field (Degenhardt et al. 2009). Studies such as these indicate that screening crop varieties for HIPV emissions and natural enemy attraction can assist in the improvement of resistant crop varieties and biological control.

Despite the exciting potential for indirect defenses to enhance pest suppression, crop breeding efforts typically focus primarily on screening for direct defenses that target pest physiology and behavior (Peterson et al. 2016, Cortesero et al. 2000, Stout 2012). Screening for genetic variation in the emission of HIPVs and attraction to natural enemies has been suggested as a means to improve the success of biological control and assist in the identification of resistance traits that can be bred into crops (Penaflor and Bento 2013, Stenberg et al. 2015). For example, olfactometer choice assays using 146 maize genotypes provided parasitoid preference data for a genome-wide association study that identified genetic loci associated with indirect defense traits (Tamiru et al. 2020). Quantifying intraspecific variation in indirect defense traits is crucial to the identification of genetic markers for future selection for indirect defenses by crop breeders. Moreover, indirect defenses can act synergistically with direct defenses that are already present in some crop species and multiple sources of defense can decrease the ability of herbivores to overcome them (Broekgaarden et al. 2011, Fatouros et al. 2014).

The sorghum aphid (Melanaphis sorghi Theobald, formerly known as the sugarcane aphid Melanaphis sacchari Zehntner), is a significant insect pest in sorghum (Sorghum bicolor L.) in North America (Nibouche et al. 2021, Kerns et al. 2015). Feeding by the sorghum aphid has caused substantial yield loss and a reduction in grain quality resulting in millions of dollars in economic damage (Knutson et al. 2016, Zapata et al. 2018). Initial pest management for the sorghum aphid relied heavily on insecticides, which was costly and can lead to insecticide resistance (Zapata et al. 2018, Colares et al. 2017). More recently, sorghum varieties with direct resistance have been deployed to suppress the sorghum aphid (Armstrong et al. 2015). To further develop and deploy resistant sorghum varieties, it is critical to identify traits that can effectively control this pest. Indirect defenses in response to sorghum aphid feeding have yet to be characterized in sorghum and almost nothing is known about the genotypic variability in HIPV emission and natural enemy attraction (Park et al. 2020). Furthermore, previous work has found certain sorghum varieties retain higher abundances of natural enemies and lower densities of sorghum aphids in the field, but the mechanism underlying this increased attraction of natural enemies is unknown (Szczepaniec 2018). Predator-prey models and greenhouse experiments show that some of these natural enemies, such as lady beetles and lacewings, are capable of suppressing sorghum aphids below economically relevant thresholds (Hewlett et al. 2019). Identification of attractive sorghum varieties has the potential to enhance pest suppression provided by a diverse range of naturally occurring predators and parasitoids (Faris et al. 2022).

To determine what sorghum cultivars have the potential to improve biological control, the goal of this study was to quantify variation in aphid-induced indirect defenses in ten sorghum cultivars. Our objectives were: (i) quantify variation in volatile emissions in plants induced by sorghum aphids and (ii) determine if variation in HIPV emission results in differences in attraction of a parasitoid of the sorghum aphid, Aphelinus nigritus, and a predator, Chrysoperla rufilabris. We posit that these screens will identify attractive sorghum cultivars that have the potential to improve biological control of the sorghum aphid and can serve as resources for future crop breeding efforts to improve resistant cultivars.

Plants. A total of 10 cultivars of sorghum – eight hybrids and two inbred lines - were used for this study. Eight of these were from the Texas A&M AgriLife Research Sorghum Improvement Program. Four of these cultivars (2 hybrids, ATx3408/RTx436 and ATx3409/RTx436, and two inbred lines, BTx3408 and BTx3409) exhibit direct resistance against the greenbug and sorghum aphids, whereas four other hybrids (ATx631/RTx436, ATx645/RTx436, BTx631, and BTx645) are susceptible to aphid infestations (Mbulwe et al. 2016, Armstrong et al. 2015). The remaining two commercial hybrids are products of Bayer®: DKS38-16 and DKS37-07 which are respectively susceptible and resistant to aphid infestations (Szczepaniec 2018). Experimental and commercial sorghum lines were selected based on differences in their lineage, such that our experiments would capture some genetic diversity in indirect defense traits.

Two seeds were planted per pot (7 cm in diameter x 6.5 cm depth) in Pro-Mix LP15 growing medium (Premier Tech Horticulture, Quakertown, Pennsylvania) and thinned to one plant after about 1 week. Plants were grown at 28–32℃ with supplemental light (16:8 light:dark cycle). Sorghum seedlings used in the volatile collections and olfactometer bioassays were grown until there were 4–6 true leaves, taking approximately 3 weeks after planting. All sorghum was watered ad libitum when the soil was dry.

Insects. Sorghum aphid colonies were established with aphids collected from sorghum in College Station, Texas in June of 2020. Colonies were maintained on DKS38-16 sorghum cultivar plants in a growth chamber (Percival Scientific Inc., Perry, Iowa) at 30℃, 40% RH, and 12:12 light:dark photoperiod. New sorghum plants were added to the colony every other day to maintain aphid abundances throughout the study. For the choice assays, we selected natural enemies that are highly correlated with sorghum aphids in sorghum (Maxson et al. 2019, Szczepaniec 2018, Faris et al. 2022). Typically, adult lacewings are used to assess natural enemy attraction to HIPVs. In this study, we chose to use larval lacewings for several reasons: 1) Chrysoperla rufilabris larvae, not adults, are predators of aphids, 2) larval lacewings can be bought in large, cost-effective numbers that are easy to maintain, and 3) our previous research has demonstrated that larval C. rufilabris are capable of significant suppression of aphids (Hewlett et al. 2019).

A. nigritus mummies were collected from sorghum aphid colonies on sorghum in College Station, TX in June of 2020. The parasitoid colony, maintained on sorghum aphid-infested DKS38-16 plants, was kept in an environmental chamber 16:8 light:dark photoperiod, 23–26℃, and 70–75% RH. Mummies were placed in petri dishes and checked daily for emergence. C. rufilabris eggs were obtained from ARBICO Organics (Oro Valley, AZ, USA). The lacewings were reared in a growth chamber set to 27, 75% RH, and 12:12 light:dark photoperiod. Eggs were separated into plastic cups and upon hatching, larvae were separated using a paintbrush. Larvae were then individually placed into their own plastic cups and fed approximately 100 aphids per day. Larvae were reared to the third instar before use in the olfactometer assays.

Olfactometer Assays. To assess natural enemy preference, a Y-tube olfactometer (ARS Gainesville, FL, OLFM-ADS-2AFM1C) was used. Two natural enemy species, parasitoid A. nigritus and predator C. rufilabris were used for this study. After assessing parasitoid responses to all ten of the sorghum cultivars, we selected two cultivars of interest (DKS37-07 and ATx3408/RTx436) to assess attraction of a predator and determine if this would match that of the parasitoid. Each replicate of the choice assay featured a pair of sorghum plants of the same cultivar, one with aphids and one without aphids. Sorghum plants at the 4–6 leaf stage were infested with 100 aphids 48 h before the start of the choice experiments. Aphids were re-counted 24 h after initial infestation and aphids were supplemented or removed to ensure that a consistent number remained on the sorghum plant. Virgin female adult A. nigritus (16 − 14 h old) and third instar C. rufilabris were starved 24 h before the start of the experiment. Airflow entering the olfactometer was drawn through activated charcoal, purified before entering the y-tube, and maintained at 15 psi. A pair of potted plants of the same cultivar with and without aphids were placed in the two 4 L glass chambers. An individual natural enemy was then placed individually into the base of the y-tube. The natural enemy was observed for 5 min and the arm choice was recorded. If the individual did not select a path (a path was considered selected once the natural enemy is ¾ way up an arm) after 5 min, “no choice” was recorded. After each trial, the y-tube was rinsed with 70% ethanol, rinsed with distilled water, and blown dry with a hair dryer. Placement of infested and un-infested plants were alternated between the two glass jars.

Volatile Collections. All 10 of the sorghum cultivars were used for volatile emission collections. Sorghum seedlings were infested with 100 aphids or remained aphid-free. To ensure the correct number of aphids were present, plants assigned to the herbivory treatment were kept in a single rearing tent and aphids were re-counted 24 h after infestation. If needed, aphids were added or removed so that all herbivory treatment plants had approximately 100 aphids. Rearing tents were kept at least one meter apart to prevent volatile-mediated interactions among plants. Collections were performed in walk-in growth rooms (28°C; 16:8 light:dark cycle; 25% RH). Individual plants were placed in heat-resistant oven bags (Reynolds Consumer Products, Lake Forest, Illinois) that were sealed at the base of the plant with a twist tie. Prior to this, oven bags were baked (150℃, 8 h) to remove caprolactam volatiles (Stewart-Jones and Poppy 2006, Derstine et al. 2020). Air was filtered and pumped into the oven bags at 200 mL min^− 1 while a vacuum pump pulled air out of the oven bags at the same time at 200 mL min^− 1. Volatiles were pulled into volatile filter traps containing 45 mg HayeSep® Q (Hutchison Hayes Separation Inc., Houston, Texas) and volatile collections lasted 8 h (09:00–17:00). Volatiles were eluted from the volatile filter traps with 150 µl of dichloromethane and each sample contained 5 µl (400 ng) of a nonyl acetate standard. Plants were cut at the base of the stem and wrapped in aluminum foil to be dried in an oven (150℃, 24 h) and dry mass was recorded for each plant.

Volatiles were quantified using an Agilent 7890 gas chromatograph (GC) and 5977B mass spectrometer. A 1 µl aliquot was injected into the column (HP-5MS 30 m x 0.250 mm-ID, 0.25 µm film thickness, Agilent Technologies). After injection, the column was held at 40℃ for 5 min, then increased 20℃/min^− 1 to 250℃. Helium was used as the carrier gas. The mass spectrometer used electron impact ionization to ionize compounds at 70 eV and produced mass spectra by scanning from 40 to 300 m/z. Tentative identification of volatile compounds were made by comparison with mass spectral libraries (NIST17, Adams2) and confirmed where possible using authentic standards (Grunseich et al. 2020). The relative abundance of each compound in ng was calculated based on the internal standard. Concentrations of volatile compounds were determined by dividing this number by the dry weight of the plant.

Statistical Analysis. All analyses were completed using R (R Version 4.2.2, R Core Team 2022). To test the null hypothesis that natural enemies had no preference for either aphid-infested or un-infested plants (i.e., a preference for one of the two olfactometer arms), chi-square tests were conducted. Total volatile emissions were calculated for each sample and log transformed to meet assumptions of homoscedasticity and normality. A two-way ANOVA was used to determine the effects of cultivar and aphid infestation on total volatile emission. To visualize and qualitatively compare HIPV blends, non-metric multidimensional scaling (NMDS) and Bray-Curtis dissimilarity metrics with the R package vegan were used (Oksanen et al. 2020). A permutational analysis of variance (PERMANOVA; number of permutations performed = 999) was used to test the hypothesis that volatile blends differed among aphid-infested sorghum cultivars using the R package vegan and the function adonis (Oksanen et al. 2020, Grunseich et al. 2020).

Random forest analyses and variable selection using the Boruta algorithm (packages: randomForest and Boruta) were used to determine which individual compounds differed most between treatments (infested and un-infested plants of the same cultivar) and among all aphid-infested cultivars (Liaw and Winer 2002, Kursa and Rudnicki 2010). Random forest analysis is a multivariate technique that creates many decision trees via bootstrapping (Breiman 2001) and is used for the classification of volatile datasets and identification of volatiles that best discriminate among groups or treatments (Ranganathan and Borges 2010). Random forest is useful for volatile datasets, as it can utilize non-parametric data, is robust to correlations among variables, can be used when there are more variables than number of samples, and is not biased toward abundant compounds (Ranganathan and Borges 2010, McCormick et al. 2014). Volatile compounds that were predicted to be different among treatments (infested vs. un-infested plants) were then analyzed by Mann-Whitney tests to determine if the amounts of volatiles changed after induction with aphid herbivory. Volatiles predicted to be different among aphid-infested cultivars were further analyzed by Kruskal-Wallis and mean separation Dunn tests to determine if the amounts of volatiles different among cultivars.

Volatiles. Across the 10 sorghum varieties, a total of 41 different volatiles were produced constitutively or were induced by aphid herbivory (Table S1). Sorghum cultivar had a significant effect on total volatile emission (F_9,209=5.89, P < 0.001) (Fig. 1a), but aphid infestation did not (F_1,209=0.67, P = 0.35). Moreover, the interaction between the effects of sorghum cultivar and aphid infestation on total volatile production was not significant (F_{9, 209}=1.12, P = 0.35) (Fig. 1b).

The production of specific volatiles, however, was affected by aphid infestation. Random forest analysis and variable selection identified specific volatiles within a cultivar that changed in their emission upon aphid infestation (Table 1).

Table 1

*Random Forest and Boruta variable selection analyses comparing infested and un-infested plants of the same cultivar*
Cultivar	Compound	Boruta IMP Factor	MW Test Statistic	P
DKS3707	benzaldehyde	5.36	59	0.0117
DKS3707	MeSA	10.13	168	0.0009
ATx3409/RTx436	MeSA	3.86	80	0.0381
BTx3409	benzaldehyde	1.79	4	0.109
BTx3409	hexadecane	3.25	4	0.176
BTx3409	linalool	3.91	17	0.0811
BTx3409	pentadecane	3.70	4	0.171
ATx3408/RTx436	1-heptadecene	3.75	42	0.0532
ATx3408/RTx436	DMNT	11.50	109.5	0.0009
BTx3408	d-limonene	4.26	157.5	0.0458
BTx3408	DMNT	4.22	176	0.0227
BTx3408	hexadecane	3.04	160	0.0601
BTx3408	octadecane	5.99	168	0.0065
BTx645	octadecane	4.49	49	0.106
BTx645	tetradecane	2.12	50	0.122
ATx631/RTx436	decane	5.27	20	0.0087
ATx631/RTx436	hexenal	3.69	33	0.0272
ATx631/RTx436	undecane	3.41	27	0.0365

For example, aphid-infested DKS37-07 released higher levels of methyl salicylate (MeSA) (Mann-Whitney U: W = 168, P = 0.01; Fig. 2a) and lower levels of benzaldehyde (Mann-Whitney U: W = 59, P < 0.001; Fig. 2b) compared to plants of this cultivar without aphids. Similarly, ATx3409/RTx436 showed increased emission of MeSA after herbivory (Mann-Whitney U: W = 80, P < 0.05; Fig. 2c). ATx3408/RTx436 and BTx3408 also showed differences in HIPV emission after herbivory. ATx3408/RTx436 emitted more DMNT after aphid herbivory (Mann-Whitney U: W = 109, P < 0.001; Fig. 2d), while BTx3408 emitted more d-limonene (Mann-Whitney U: W = 157, P < 0.05), DMNT (Mann-Whitney U: W = 176, P < 0.05), and octadecane (Mann-Whitney U: W = 168, P < 0.01) (Fig. 2e, f, g). In contrast, aphid herbivory decreased emissions of decane (Mann-Whitney U: W = 20, P < 0.01), hexenal (Mann-Whitney U: W = 33, P < 0.05), and undecane (Mann-Whitney U: W = 27, P < 0.05) (Fig. 2h, i, j) in ATx631/RTx436.

Aphid-induced volatile blends differed significantly among varieties (PERMANOVA: pseudo-F_9,199=4.068, P = 0.001; Fig. S1). Random forest analysis showed that multiple terpenes, alkanes, and aromatic compounds were important for distinguishing among aphid-infested cultivars (Table 2, Fig. 3).

Table 2

*Random forest and Boruta variable selection analyses compared volatile blends across aphid-infested varieties*
Compound	Boruta IMP Factor	KW Test Statistic	P
ß-farnesene	7.332218762	25.11	0.002
1-heptadecene	10.11402016	44.57	< 0.0001
α-pinene	12.00700396	26.88	< 0.001
benzaldehyde	10.08400598	26.58	< 0.001
d-Limonene	5.114639587	20.93	0.01
DMNT	16.31860182	58.07	< 0.0001
heptadecane	10.41462375	43.04	< 0.0001
hexadecane	8.859449019	37.87	< 0.0001
hexanal	5.899953749	36.92	< 0.0001
linalool	11.31278871	42.67	< 0.0001
MeSA	7.767129873	29.66	0.001
pentadecane	5.940673135	27.71	0.001

For example, BTx631 produced the highest amount of benzaldehyde (Fig. 3d). Alternatively, DMNT production was highest in two cultivars, ATx3408/RTx436 and BTx3408, but ATx3409/RTx436 produced similar amounts (Fig. 3f). While ATx3409/RTx436 produced the highest numerical amount of MeSA among all aphid-infested cultivars, ATx3408/RTx436 and BTx3408 produced similar amounts of MeSA (Fig. 3k). Notably, ATx3408/RTx436 produced the highest amount of an aldehyde, hexenal, when induced by aphids (Fig. 3i).

Olfactometer Assays. A. nigritus parasitoids showed a preference for volatiles from aphid-induced DKS37-07 (χ² = 4.16, df = 23, P < 0.05) and ATx3409/RTx436 (χ² = 14.44, df = 12, P < 0.001) (Fig. 4). Parasitoids showed no preference between plants with or without aphids in sorghum cultivars BTx3409 (χ² = 0, df = 11, P = 1), ATx645/RTx436 (χ² = 0.06, df = 14, P = 0.55), BTx631 (χ² = 0.06, df = 14, P = 0.54), and DKS38-16 (χ² = 0.04, df = 24, P > 0.05). In contrast, parasitoids preferred volatiles from some cultivars without aphids, including ATx3408/RTx436 (χ² = 5.76, df = 12, P < 0.05), BTx3408 (χ² = 7.84, df = 13, P < 0.01), ATx631/RTx436 (χ² = 11.56, df = 14, P < 0.001), and BTx645 (χ² = 64, df = 8, P < 0.001).

Third instar C. rufilabris were also attracted to aphid-infested DKS37-07 (χ² = 3.8, df = 30, P < 0.05) (Fig. 5) while larval lacewings preferred un-infested ATx3408/RTx436 plants over aphid-infested plants (χ² = 3.9, df = 30, P < 0.05).

Our results demonstrate there was significant variation in the composition of volatiles among sorghum varieties and this, in turn, affected the behavior of natural enemies. The total amount of volatiles emitted was not different across the 10 sorghum varieties. However, the composition of HIPVs emitted from the varieties differed, with some varieties showing increases or decreases of specific volatile compounds. Both the parasitoid and predator responded to these HIPVs in similar ways – for example, both parasitoids and larval lacewings were attracted to aphid-infested DKS37-07 over non-infested plants. Moreover, four of the ten sorghum varieties were not attractive to the natural enemies when infested with aphids. Our results, like other studies investigating genotypic variation in indirect defense (Kappers et al. 2010, Tahmaesbi et al. 2014, Krips et al. 2001), have found that differences in HIPV blends can have considerable effects on the attraction of natural enemies.

We found that total volatile emissions did not correspond to natural enemy behavior. For example, DKS37-07, an attractive cultivar produced the least volatiles overall, while BTx3409, an unattractive cultivar, produced the highest amount of volatiles. Moreover, aphid herbivory was not a significant factor that affected the total amount of volatiles emitted – this does not explain why some un-infested varieties (e.g., ATx3408/RTx436) were attractive to natural enemies. These results are like other studies, wherein natural enemy responses to herbivore-infested plants could not be predicted by total volatile emissions, but instead by the composition of the HIPV blends (Degen et al. 2012, Lou et al. 2006). For instance, the parasitoid Cotesia marginiventris could distinguish between maize cultivars that produced similar amounts of total volatiles in olfactometer bioassays, indicating that the quality of the HIPV blend determined parasitoid preference (Hoballah et al. 2002). In the current study, whether sorghum plants were infested with aphids or not, the plants produced relatively low levels of volatiles. Total volatile emission did not exceed 1,000 ng/g of dried plant tissue.

The composition of HIPV blends is important for attraction of natural enemies and our results indicate that some varieties show significant changes in specific volatiles upon aphid herbivory. For example, emission of MeSA increased after herbivory in two sorghum cultivars (DKS37-07 and ATx3409/RTx436), which were attractive to the natural enemies when infested with aphids. MeSA has been shown to be an important attractant for a diverse array of natural enemies in the laboratory and field (De Boer and Dicke 2004, Rodriguez-Saona 2011a). While MeSA appears to be an important volatile for attraction of natural enemies to these two varieties, it is unlikely that it is the sole attractant for the parasitoid and predator. Aphid-infested BTx3408 plants, which were not preferred by natural enemies, produced similar amounts of MeSA as induced DKS37-07 and ATx3409/RTx436 plants. However, it has been shown that a mixture of volatile compounds can be more attractive to natural enemies than singular volatile compounds (Kaplan 2012). In the case of predatory mite Phytoseiulus persimilis, attraction to individual compounds such as MeSA or cis-3-hexen-1-ol was low compared to the full HIPV blend from the lima bean plant (van Wijk et al. 2011). Other co-occurring changes in the volatile blend may be responsible for differences in attraction; in the case of DKS37-07, benzaldehyde emission decreases in aphid-attacked plants.

Surprisingly, for certain sorghum varieties, natural enemies preferred un-infested plants over aphid-infested plants. These varieties also had distinct HIPV blends – for example, ATx3408/RTx436 was the only cultivar that had increased hexenal emissions upon aphid herbivory. Furthermore, ATx3408/RTx436 and BTx3408 had increase emissions of the terpenoid compound (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT) after aphid herbivory. DMNT has been found to be attractive to natural enemies such as spider mites and lacewings (Dicke et al. 1990, Hedge et al. 2011), but several studies have shown that changes in specific volatiles within a blend can alter attractiveness to natural enemies (Snoeren et al. 2010, Loivamaki et al. 2008, D’Alessandro et al. 2006). For example, cucumber varieties that produced higher proportions of methyl salicylate, geranyl isovalerate, or α-patchoulene were less attractive to predatory mites compared to other cucumber varieties that emitted compounds such as (E)-beta-ocimene and (E,E)-TMTT (Kappers et al. 2011). While it is counter-intuitive for plants to emit HIPV blends that are not attractive to natural enemies, Kappers et al. (2011) hypothesized that plant volatiles that repel natural enemies may play other important roles in defense that still benefit the plant, like microbial resistance (Huang et al. 2012). DMNT, for example, has been previously shown to play a role in resistance against a root rot pathogen Phythium irregulare in Arabidopsis (Sohrabi et al. 2015). Ultimately, it is unclear which specific sorghum HIPVs play a role in repellence of natural enemies and further work should be done to determine if compounds such as DMNT and hexenal cause such behaviors.

Alternatively, it is possible that sorghum aphids modulate indirect defenses to their benefit by repelling natural enemies. Aphids and other sap feeders are known to induce salicylic acid-mediated defenses, which can interfere with JA-mediated defenses (Thaler et al. 2012). In 2- and 6-week old sorghum seedlings, sorghum aphid herbivory induced changes in gene expression – in particular, genes from the jasmonate ZIM-domain (JAZ) family, which are known to repress JA-mediated responses, were upregulated (Kiani and Szczepaniec 2018). It has been suggested that aphids may modulate crosstalk, thereby suppressing indirect defenses like JA-mediated production of HIPVs (Walling 2008). Thus, aphid herbivory has the potential to elicit quantitative changes of individual volatiles within a blend, thereby affecting natural enemy attraction (Schwartzberg et al. 2010, Frago et al. 2017). Use of certain varieties has the potential to be particularly detrimental to pest control efforts, as we have identified aphid-infested varieties (e.g., ATx631/RTx436 and BTx645) that are both susceptible to aphid herbivory and could not recruit natural enemies in laboratory assays.

Current methods for sorghum aphid control rely mainly on spraying insecticides. The continued use of these insecticides is likely to lead to the development of resistant aphid populations (Colares et al. 2017). In addition, insecticide applications are costly (Zapata et al. 2016) and integrated tactics for pest management are necessary to reduce economic losses (Haar et al. 2019). Currently, no biological control agents are sold commercially for this system and partially resistant cultivars can still allow for sorghum aphid colonies to persist (Gordy et al. 2021). In this research, we demonstrated that variation in HIPVs can lead to variation in natural enemy attraction. Further studies should investigate and confirm which volatile compounds are important for the attraction of natural enemies via laboratory bioassays (Penaflor et al. 2011). There have been efforts to identify specific attractive HIPVs to create artificial volatile lures – while some studies confirm that these lures can attract significantly higher abundances of natural enemies, there is little evidence that these lures enhance predation of pests (Lee et al. 2021). Alternatively, screening and selecting crop varieties for indirect defenses can enhance the efficacy of biological control on pest suppression, such that planting attractive crop varieties can enhance natural enemy attraction (Penaflor and Bento 2013, Stenberg et al. 2015). Moreover, field testing is necessary, as laboratory assays may not always translate to attraction of natural enemies in the field (Salamanca et al. 2017). Field studies using “attractive” plant varieties have been promising, with attractive varieties demonstrating higher parasitism rates (Rasmann et al. 2005). For example, a Brassica oleracea cultivar emitting significantly higher amounts of MeSA attracted more parasitoids from farther distances than other, less attractive cultivars and caterpillars on these plants were parasitized at a significantly higher rate (Poelman et al. 2009, Aartsma et al. 2018). We conclude that indirect defenses in sorghum are an overlooked yet important component of plant resistance, and variation in HIPV emissions have potential applications in improvement of biological control.

ACKNOWLEDGEMENTS

We would like to thank members of the Eubanks, Helms, and Rooney laboratories for their assistance on this work. Thank you to Morgan Thompson for your contributions in discussions about the manuscript. This work was supported by funds from the USDA National Institute of Food and Agriculture, Hatch project COL00411 (AS), USDA NIFA 2019-05262 (AS and MDE), and an National Science Foundation Graduate Research Fellowship (EMR).

AUTHOR CONTRIBUTIONS

Research was planned by EMR, AS, WLR, AMH, and MDE. EMR, JAH, and JMG collected, recorded, and analyzed data. EMR wrote drafts of the manuscript. The final manuscript was reviewed by JAH, JMG, AS, WLR, AMH, and MDE. All the authors read and approved the final manuscript.

Competing interests. The authors have no competing interests to declare that are relevant to the content of this article.

FUNDING DECLARATION

This work was supported by funds from the USDA National Institute of Food and Agriculture, Hatch project COL00411 (AS), USDA NIFA 2019-05262 (AS and MDE), and a National Science Foundation Graduate Research Fellowship (EMR).

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No competing interests reported.

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Indirect Defense in Sorghum: Attraction of Natural Enemies to Aphid-Infested Plants Varies among Cultivars

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